Fungal Schizophrenia: What The Colletotrichum Genome Tells Us About The Biotrophic-Necrotrophic Switch

The fungal genus Colletotrichum contains at least 600 species that are pathogenic on more than 3000 plant species.  Colletotrichum pathogens are hemibiotrophic, initiating infection from melanized appressoria as intracellular biotrophs, and later switching to necrotrophic growth that degrades host tissues and produces visible lesions.  We sequenced and compared the genomes and the in planta transcriptomes of two related species, C. higginsianum which infects Arabidopsis and other Brassicaceae, and C. graminicola, which is specific to maize.  Both species encoded large numbers of potential pathogenicity-related proteins, including putative secreted effectors, secondary metabolism enzymes, and cell wall degrading enzymes.  The large variety and number of these genes resembled the genetic repertoire of necrotrophic fungi more than that of biotrophs. Transcriptome analysis revealed that effectors and secondary metabolism enzymes were preferentially expressed prior to infection and during the biotrophic phase, while cell wall degrading enzymes and transporters were upregulated later at the switch to necrotrophy.  This suggests that the appressorium and biotrophic hyphae function primarily as secretory organs for compounds that induce host susceptibility, while the majority of nutrient uptake from the host occurs after the switch to necrotrophy. Comparisons of gene expression in C. higginsianum appressoria in vitro versus in planta revealed that more than 1500 genes were induced by plant signals.  Both species encoded more than 500 transcription factors, which were expressed in sequential waves during the penetration and colonization process.  Evaluation of expression patterns may reveal which transcription factors are most important in the transition from biotrophy to necrotrophy.